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Successive changes in tissue migration capacity of developing larvae of an intestinal nematode, Strongyloides venezuelensis

Published online by Cambridge University Press:  09 November 2005

H. MARUYAMA ,
A. NISHIMAKI ,
Y. TAKUMA ,
M. KURIMOTO ,
T. SUZUKI ,
Y. SAKATOKU ,
M. ISHIKAWA  and
N. OHTA
H. MARUYAMA
Affiliation:
Department of Molecular Parasitology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, Mizuho-cho, Mizuho, Nagoya 467-8601, Japan
A. NISHIMAKI
Affiliation:
Department of Molecular Parasitology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, Mizuho-cho, Mizuho, Nagoya 467-8601, Japan
Y. TAKUMA
Affiliation:
Department of Molecular Parasitology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, Mizuho-cho, Mizuho, Nagoya 467-8601, Japan
M. KURIMOTO
Affiliation:
Department of Molecular Parasitology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, Mizuho-cho, Mizuho, Nagoya 467-8601, Japan
T. SUZUKI
Affiliation:
Department of Molecular Parasitology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, Mizuho-cho, Mizuho, Nagoya 467-8601, Japan
Y. SAKATOKU
Affiliation:
Department of Molecular Parasitology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, Mizuho-cho, Mizuho, Nagoya 467-8601, Japan
M. ISHIKAWA
Affiliation:
Department of Molecular Parasitology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, Mizuho-cho, Mizuho, Nagoya 467-8601, Japan
N. OHTA
Affiliation:
Department of Molecular Parasitology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, Mizuho-cho, Mizuho, Nagoya 467-8601, Japan
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Abstract

Infective larvae of an intestinal nematode, Strongyloides venezuelensis, enter rodent hosts percutaneously, and migrate through connective tissues and lungs. Then they arrive at the small intestine, where they reach maturity. It is not known how S. venezuelensis larvae develop during tissue migration. Here we demonstrate that tissue invasion ability of S. venezuelensis larvae changes drastically during tissue migration, and that the changes are associated with stage-specific protein expression. Infective larvae, connective tissue larvae, lung larvae, and mucosal larvae were used to infect mice by various infection methods, including percutaneous, subcutaneous, oral, and intraduodenal inoculation. Among different migration stages, only infective larvae penetrated mouse skin. Larvae, once inside the host, quickly lost skin penetration ability, which was associated with the disappearance of an infective larva-specific metalloprotease. Migrating larvae had connective tissue migration ability until in the lungs, where larvae became able to settle down in the intestinal mucosa. Lung larvae and mucosal larvae were capable of producing and secreting adhesion molecules.

Keywords

Strongyloides venezuelensisintestinal nematodemigrationdevelopmentlarva
Type
Research Article
Information
Parasitology , Volume 132 , Issue 3 , March 2006 , pp. 411 - 418
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Blaxter, M. ( 2003). Nematoda: genes, genomes and the evolution of parasitism. Advances in Parasitology 54, 101–195.CrossRefGoogle Scholar
Brindley, P.J., Gam, A. A., McKerrow, J. H. and Neva, F. A. ( 1995). Ss40: the zinc endopeptidase secreted by infective larvae of Strongyloides stercoralis. Experimental Parasitology 80, 1–7.CrossRefGoogle Scholar
Crook, M., Thompson, F. J., Grant, W. N. and Viney, M. E. ( 2005). daf-7 and the development of Strongyloides ratti and Parastrongyloides trichosuri. Molecular and Biochemical Parasitology 139, 213–223.CrossRefGoogle Scholar
Daly, C. M., Mayrhofer, G. and Dent, L. A. ( 1999). Trapping and immobilization of Nippostrongylus brasiliensis larvae at the site of inoculation in primary infections of interleukin-5 transgenic mice. Infection and Immunity 67, 5315–5323.Google Scholar
Dent, L. A., Daly, C. M., Mayrhofer, G., Zimmerman, T., Hallett, A., Bignold, L. P., Creaney, J. and Parsons, J. C. ( 1999). Interleukin-5 transgenic mice show enhanced resistance to primary infections with Nippostrongylus brasiliensis but not primary infections with Toxocara canis. Infection and Immunity 67, 989–993.Google Scholar
Dorris, M., Viney, M. E. and Blaxter, M. L. ( 2002). Molecular phylogenetic analysis of the genus Strongyloides and related nematodes. International Journal for Parasitology 32, 1507–1517.CrossRefGoogle Scholar
Gold, D., Stein, B. and Tzipori S. ( 2001). The utilization of sodium taurocholate in excystation of Cryptosporidium parvum and infection of tissue culture. Journal of Parasitology 87, 997–1000.CrossRefGoogle Scholar
Gomez Gallego, S., Loukas, A., Slade, R. W., Neva, F. A., Varatharajalu, R., Nutman, T. B. and Brindley, P. J. ( 2005). Identification of an astacin-like metallo-proteinase transcript from the infective larvae of Strongyloides stercoralis. Parasitology International 54, 123–133.CrossRefGoogle Scholar
Kinjo, T., Tsuhako, K., Nakazato, I., Ito, E., Sato, Y., Koyanagi, Y. and Iwamasa, T. ( 1998). Extensive intra-alveolar haemorrhage caused by disseminated strongyloidiasis. International Journal for Parasitology 28, 323–330.CrossRefGoogle Scholar
Kita, K. and Takamiya, S. ( 2002). Electron-transfer complexes in Ascaris mitochondria. Advances in Parasitology 51, 95–131.CrossRefGoogle Scholar
Maruyama, H., El-Malky, M., Kumagai, T. and Ohta, N. ( 2003). Secreted adhesion molecules of Strongyloides venezuelensis are produced by oesophageal glands and are components of the wall of tunnels constructed by adult worms in the host intestinal mucosa. Parasitology 126, 165–171.CrossRefGoogle Scholar
Maruyama, H., Nawa, Y. and Ohta, N. ( 1998). Strongyloides venezuelensis: Binding of orally secreted adhesion substances to sulfated carbohydrates. Experimental Parasitology 89, 16–20.CrossRefGoogle Scholar
Maruyama, H., Yabu, Y., Yoshida, A., Nawa, Y. and Ohta, N. ( 2000). A role of mast cell glycosaminoglycans for the immunological expulsion of intestinal nematode, Strongyloides venezuelensis. Journal of Immunology 164, 3749–3754.CrossRefGoogle Scholar
McKerrow, J. H., Brindley, P., Brown, M., Gam, A. A., Staunton, C. and Neva, F. A. ( 1990). Strongyloides stercoralis: identification of a protease that facilitates penetration of skin by the infective larvae. Experimental Parasitology 70, 134–143.CrossRefGoogle Scholar
Mohrlen, F., Hutter, H. and Zwilling, R. ( 2003). The astacin protein family in Caenorhabditis elegans. European Journal of Biochemistry 270, 4909–4920.CrossRefGoogle Scholar
Takamure, A. ( 1995). Migration route of Strongyloides venezuelensis in rodents. International Journal for Parasitology 25, 907–911.CrossRefGoogle Scholar
Tsuji, N. and Fujisaki, K. ( 1994). Development in vitro of free-living infective larvae to the parasitic stage of Strongyloides venezuelensis by temperature shift. Parasitology 109, 643–648.CrossRefGoogle Scholar
Tsuji, N., Kawazu, S., Nakamura, Y. and Fujisaki, K. ( 1993). Protein analysis of Strongyloides venezuelensis by two-dimensional polyacrylamide gel electrophoresis. Journal of Veterinary Medical Sciences 55, 881–883.CrossRefGoogle Scholar
Wertheim, G. ( 1970). Growth and development of Strongyloides venezuelensis Brumpt, 1934 in the albino rat. Parasitology 61, 381–388.CrossRefGoogle Scholar
Zhan, B., Hotez, P. J., Wang, Y. and Hawdon, J. M. ( 2002). A developmentally regulated metalloprotease secreted by host-stimulated Ancylostoma caninum third-stage infective larvae is a member of the astacin family of proteases. Molecular and Biochemical Parasitology 120, 291–296.CrossRefGoogle Scholar